Abstract
Purpose
Sudden cardiac death after ejaculation has been reported in humans and highlights the important relationship between sexual behavior and the heart. The rat is an extremely useful animal model for investigating reproductive function in male mammals. In this study, we examined the relationship between autonomic nervous system activity and the circulatory system during sexual behavior in male rats.
Methods
Male Wistar–Imamichi rats were exposed to female rats in estrous and heart rate (HR), systolic blood pressure (SBP), diastolic blood pressure (DBP), and plasma noradrenaline (NA) and adrenaline (Ad) concentrations were measured by telemetry during copulation.
Results
The resting HR was 365.5 ± 18.4 beats/min (mean ± SE), which increased to 531.2 ± 21.1 beats/min at ejaculation and decreased to 404.6 ± 30.7 beats/min 1 min after ejaculation. At rest, SBP and DBP were 123.8 ± 6.6 and 81.5 ± 4.1 mmHg, respectively, which increased to 154.5 ± 5.9 and 112.1 ± 7.3 mmHg at ejaculation. Baseline plasma Ad and NA concentrations were 151.6 ± 32.0 and 248.5 ± 22.5 pg/ml, respectively, and these increased to 393.8 ± 89.9 and 792.7 ± 154.0 pg/ml at ejaculation, after which they decreased to resting levels. The rate of increase in NA at ejaculation differed significantly from that of Ad.
Conclusions
The load on the circulatory and autonomic nervous systems is controlled by a rapid decrease in HR and NA concentration immediately after ejaculation, such that the male rat is prepared for the next copulation.
Keywords: Blood pressure, Catecholamines, Ejaculation, Heart rate, Rat copulation
Introduction
Previous reports of sudden cardiac death after ejaculation indicate an important relationship between male sexual behavior and the circulatory system [1]. Ejaculation is the most important reproductive function of the mammalian male and understanding its mechanism will help improve reproductive technologies and the treatment of reproductive disorders. In addition, elucidating the relationship between ejaculation and the heart will contribute to safer reproductive behavior.
Sexual behavior in mammals is controlled by the autonomic nervous system, the somatic nerves, and various endocrine factors [2, 3, 4], but their interrelationships remain unclear. The rat is an extremely useful animal model to investigate reproductive function in male mammals. Notably, no previous study has investigated copulatory behavior using a pharmacological or neuroendocrinological approach. In this study, we measured heart rate (HR), systolic (SBP) and diastolic blood pressure (DBP), and the plasma concentrations of noradrenaline (NA) and adrenaline (Ad) in the male rat during copulation.
Materials and methods
Animals
Male Wistar–Imamichi rats aged nine weeks and female Wistar–Imamichi rats aged nine to twelve weeks were acclimatized under controlled conditions in an animal room (12‐h light/dark cycle, 24°C), with ad libitum access to food and water for at least a week prior to experimentation.
Cannulation and implantation of the transmitter
One week before the experiment, male rats were anesthetized with pentobarbital sodium, the right femoral vein was exposed, and the tip of a catheter for collecting blood (CNC‐3.5H; Access Technologies, Skokie, IL, USA) was advanced into the caudal vena cava. The external end of the catheter (POR AC‐3.5H; Access Technologies) was tunneled under the skin to the back of the neck and fixed. The catheter was flushed and then filled with heparinized saline (20 IU/ml). A telemetric transmitter for HR and BP measurements (TA11PA‐C40; Data Sciences, St Paul, MN, USA) was immersed in sterile saline at room temperature for 10 min prior to surgery and implanted using the following procedure. The abdominal aorta was separated from the caudal vena cava through a 5‐cm laparotomy incision and then lifted clear using a length of suture thread passed under each end. Tension was maintained on the sutures to occlude blood flow and a sterile 21‐gauge needle, with its tip bent up at a 45° angle, was used to puncture the artery wall and introduce the implant catheter (0.7‐mm diameter), which was directed proximally. The catheter entry point was bonded (Vetbond; 3M, St Paul, MN, USA) to ensure that the pressure‐sensing tip would remain in the proper position to retrieve data. The telemetry implant was fixed with sutures and the skin incision was closed.
After surgery, male rats were housed individually and the catheter was flushed with heparinized saline every day for a week.
Observation of sexual behavior and data recording
A special needle joined to a tube with two syringes (PG 22‐75; Access Technologies) was fixed to the end of the catheter in each male rat, and the rat was placed in a cylindrical observation cage (diameter, 300 mm; height, 330 mm) on a signal‐receiving board (RA1310, Data Sciences). After 30 min, a female rat in estrous was put into the cage and sexual behavior was observed under a red light.
HR, SBP, and DBP were recorded through the signal‐receiving board every 5 s. Atmospheric pressure was continuously measured (APR‐1; Data Sciences) and blood pressure data were corrected by the system. All analyses were performed with Dataquest ART analysis software (Data Sciences).
Plasma noradrenaline and adrenaline concentrations
Male rats were separated into eight groups (3–5 rats each) according to blood collection time—resting within the observation cage, first intromission, ejaculation, and 1, 2, 3, 4, and 5 min after ejaculation. Each 2‐ml blood sample was collected via the catheter in the caudal vena cava using a heparinized syringe.
All blood samples were kept on ice until centrifugation at 2200 × g for 15 min at 4°C, and plasma fractions were stored at −80°C until analysis. Plasma NA and Ad concentrations were measured by high‐performance liquid chromatography (C‐R7A; Shimadzu, Tokyo, Japan) with electrochemical detection (Nanospace SI‐1 2005; Shiseido, Tokyo, Japan), as previously described [5].
Statistical analysis
All data are presented as the mean ± SE. Statistical analysis was performed using two‐way repeated analysis of variance (ANOVA) followed by Dunnett's test. Values were considered significantly different at P < 0.05.
Results
Heart rate
Figure 1 shows the changes in HR during copulation. HR was significantly higher at first intromission and ejaculation (490 ± 14.1 and 531.2 ± 21.1 beats/min, respectively) compared with the resting value of 365.5 ± 18.4 beats/min (P < 0.01). HR peaked at ejaculation and declined to 439.9 ± 5.3 beats/min 5 min later. Of the HR measurements recorded after ejaculation, only HR at 3 min after ejaculation (475.0 ± 18.6 beats/min) was significantly higher than the resting level (P < 0.05). HR values at rest and at 1 and 4 min after ejaculation were significantly lower compared with HR at ejaculation (P < 0.01 and P < 0.05, respectively).
Figure 1.
Changes in heart rate and plasma concentrations of adrenaline and noradrenaline during copulatory behavior in the male rat. Data are mean ± SE. Dunnett's test; *P < 0.05 versus value at rest, **P < 0.01 versus value at rest; † P < 0.05 versus value at ejaculation, ‡ P < 0.01 versus value at ejaculation
Plasma Ad and NA concentrations
Figure 1 shows the observed changes in plasma catecholamine concentrations during copulation. The Ad concentration tended to increase and reached its highest level at ejaculation (393.8 ± 89.9 pg/ml), but was not significantly different from the resting value (151.6 ± 32.0 pg/ml). Likewise, Ad concentrations 1, 2, 3, 4, and 5 min after ejaculation did not differ significantly from the resting or ejaculatory values.
NA concentrations at first intromission and ejaculation were significantly higher (P < 0.01) than those at rest (248.5 ± 22.5 pg/ml). At ejaculation, the NA concentration peaked at 792.7 ± 154.0 pg/ml, which was 319% higher than the resting value. NA concentrations 1, 2, 3, 4, and 5 min after ejaculation did not differ significantly from the resting value, but the concentration 1 min after ejaculation was significantly lower than that at ejaculation.
Blood pressure
SBP
The SBP at ejaculation (154.5 ± 5.9 mmHg) was significantly higher than the resting value (123.8 ± 6.6 mmHg, P < 0.01; Fig. 2). Although the SBP values 1, 2, 3, 4, and 5 min after ejaculation did not differ significantly from the resting SBP, values 2, 3, 4 and 5 min after ejaculation were significantly lower than peak SBP at ejaculation (P < 0.05, P < 0.01, respectively).
Figure 2.
Changes in systolic and diastolic blood pressure during copulatory behavior in the male rat. Data are mean ± SE. Dunnett's test; *P < 0.05 versus value at rest, **P < 0.01 versus value at rest; † P < 0.05 versus value at ejaculation, ‡ P < 0.01 versus value at ejaculation
DBP
DBP was also significantly higher at ejaculation (112.1 ± 7.3 mmHg) than at rest (81.5 ± 4.1 mmHg, P < 0.05; Fig. 2). DBP values 1, 2, 3, 4, and 5 min after ejaculation did not differ significantly from the values at rest or at ejaculation.
Discussion
We studied the relationship between the autonomic nervous system and the circulatory system during male sexual behavior by measuring HR, SBP, DBP, and plasma catecholamine concentrations in copulating male rats by using a telemetry system, which has been used to measure HR in many types of experimental animals without limiting their behavior [6, 7, 8, 9].
The male rat ejaculates after mounting and performing several intromissions of the penis [10]. In this study, HR peaked at ejaculation and decreased rapidly 1 min later (Fig. 1, P < 0.05), indicating that rapid changes in autonomic nervous activity occur during sexual behavior, as shown in our previous studies [5, 6].
Both SBP and DBP peaked at ejaculation in copulating male rats. SBP values 2, 3, 4, and 5 min after ejaculation were significantly lower than the peak level (P < 0.05, P < 0.01), but the respective DBP values did not differ significantly. SBP and DBP are affected by changes in HR and stroke volume, arterial extensibility, ejection speed, and peripheral resistance [11]. SBP, in particular, is affected by changes in stroke volume, arterial extensibility, and ejection speed, whereas DBP is affected by changes in HR, SBP, arterial extensibility, and peripheral resistance. There is a strong relationship between HR and stroke volume [11], suggesting that stroke volume decreases suddenly with HR just after ejaculation, resulting in a sudden decrease in SBP.
There is a strong correlation between plasma NA and Ad concentrations and HR [12, 13]. In this study, plasma NA and Ad concentrations peaked at ejaculation, as did HR (Fig. 1). In particular, the change in NA concentration during sexual behavior was similar to the change in HR (Fig. 1). Plasma Ad and NA concentrations at ejaculation were higher than resting values, although their rates of increase differed, which is a characteristic reaction of the sympatho‐adrenomedullary system to the exercise load of sexual behavior (i.e., tension in the sympathetic nerves leads to secretion of NA) [11, 14]. The significant increase in plasma NA concentration during sexual behavior indicates a high exercise intensity.
The male rat vocalizes at 22 kHz to avoid further contact with the female after ejaculation and there is a rapid decrease in deep body and hypothalamic temperature [15, 16, 17, 18]. These behaviors enable the rat to perform frequent copulations. Based on our current and previous findings, we suggest that the load on the heart and autonomic nervous system during male sexual behavior is controlled by a rapid decrease in HR and NA concentration immediately after ejaculation, which prepares the male for the next ejaculation series. The results of this study demonstrate characteristic activity of the sympatho‐adrenomedullary system during male sexual behavior.
Acknowledgment
This study was supported in part by Grants‐In‐Aid for Scientific Research from the Society for Encouragement of Biomedical Education, a non‐profit organization, to PK.
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